Document [original]

AGROECOSYSTEMS

Plant damage in urban agroecosystems varies with local and

landscape factors

MONIKA EGERER ,

1,3,



HEIDI LIERE ,

AZUCENA LUCATERO ,

AND STACY M. PHILPOTT

Department of Environmental Studies, University of California, Santa Cruz, California 95060 USA

Department of Environmental Studies, Seattle University, Seattle, Washington 98122 USA

Citation: Egerer, M., H. Liere, A. Lucatero, and S. M. Philpott. 2020. Plant damage in urban agroecosystems varies with

local and landscape factors. Ecosphere 11(3):e03074. 10.1002/ecs2.3074

Abstract. Biotic and abiotic factors at local to landscape scales inﬂuence insect pest and disease dynam-

ics in agricultural systems. However, relative to studies focused on the importance of these drivers of crop

plant damage in rural agricultural systems, few studies investigate plant damage from herbivore insects

and plant diseases in urban agroecosystems, and consequently, most urban farmers lack knowledge on

crop protection tactics. Here we use three common crop species within urban agroecosystems (community

gardens) distributed across an urban landscape as a model system to ask how local, landscape, and micro-

climate factors relate to herbivore and disease plant damage. We hypothesized that plant damage would

be lower in gardens with greater local vegetation complexity, landscape‐scale complexity, and less variable

temperatures, but that the importance of factors is species‐and damage‐speciﬁc. By measuring Brassica,

cucurbit, and tomato insect pest and disease damage across the growing season, we conﬁrmed that the

importance of factors varies with crop species and by damage type. Both local complexity factors (e.g.,

number of trees and shrubs) and landscape complexity (percent natural cover in the landscape) relate to

lower incidence of herbivore and disease damage on some crops, supporting our prediction that habitat

heterogeneity at both local and landscape scales lowers plant damage. Greater temperature variability

related to higher disease damage on tomatoes linking microclimate factors to disease prevalence. Yet, local

complexity factors also related to higher incidence of plant damage for other crop species, indicating vari-

able species‐level impacts of local management factors on plant damage. By measuring the abundance of

fungus‐feeding lady beetles (Psyllobora) on cucurbits, we conﬁrmed a strong association between natural

enemies and powdery mildew. We provide a case study on how changes in local to landscape‐scale factors

relate to plant damage in urban agroecosystems and suggest how urban farmers and gardeners can apply

this ecological knowledge to improve sustainable urban food production.

Key words: agroecological management; California; conservation biological control; disease; herbivory; temperature

variability; urban agriculture.

Received 8 January 2020; accepted 15 January 2020. Corresponding Editor: Debra P. C. Peters.

License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Present address: Department of Ecology, Ecosystem Science/Plant Ecology, Technische Universität Berlin,

Rothenburgstr. 12, Berlin 12165 Germany.

E‐mail: monika.egerer@tu-berlin.de

INTRODUCTION

In agricultural systems, farmers are continu-

ously challenged by a wide range of crop‐

damaging pests. Insect, bacterial, and fungal

agricultural pests cause billions of dollars of crop

damage annually (Losey and Vaughan 2006).

Both biotic and abiotic factors affect the bottom‐

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up and top‐down forces that drive pest control in

agroecosystems (Thies and Tscharntke 1999,

Gonthier et al. 2013, Liere et al. 2015). Agroeco-

logical practices aimed at preventing insect her-

bivore and plant disease outbreaks include crop

diversiﬁcation and rotation (Altieri 2004, Bom-

marco et al. 2013). Ecological principles based in

biological diversiﬁcation, closed‐loop cycling,

species interactions, and spatio‐temporal com-

plexity underlie these practices. On the one hand,

as predicted by the enemies hypothesis, increas-

ing habitat heterogeneity—by diversifying crop

composition and structure, and adding ﬂoral

resources—leads to increased natural enemy

abundance and diversity, thereby enhancing crop

pest suppression (Root 1973). On the other hand,

the resource concentration hypothesis predicts

that higher concentrations of host plants and less

vegetation diversity facilitate host plant location

ultimately leading to herbivore and disease out-

breaks. Both of these hypotheses support the

idea that local habitat heterogeneity reduces her-

bivore and disease outbreak both through herbi-

vore and disease resource manipulation, and

through increased herbivore and pathogen mor-

tality by natural enemies to enhance pest control

(Kremen and Miles 2012, Rusch et al. 2013, Marja

et al. 2018). Agroecological practices grounded

in ecological theory have potential to minimize

crop plant damage and enhance crop production

through on‐farm management of habitat struc-

ture (Garibaldi et al. 2018), but further studies

are needed.

In addition to local agroecosystem features at

the farm scale (Batáry et al. 2011), the effect of

agroecosystem management on biodiversity and

ecosystem function largely depends on land-

scape context (Tscharntke et al. 2005). In systems

embedded within simpliﬁed landscapes with less

natural habitat, agroecological management has

larger, positive effects on biodiversity and

ecosystem functions than in systems in more

complex landscapes with more natural habitat to

an extent, though the relationship is not linear.

Along with effects on herbivores and natural

enemies, landscape context may also inﬂuence

epidemic invasions and plant disease spread in

agricultural systems through habitat connectivity

(Mundt et al. 2011). Many crop diseases includ-

ing fungal pathogens and air‐borne diseases are

capable of long‐distance aerial dispersal (e.g., via

spores) across the landscape (Brown and

Hovmøller 2002). Consequently, the disease

prevalence and disease dynamics within an

agroecosystem may largely depend on surround-

ing landscape composition through dispersal

facilitation or limitation (Plantegenest et al.

2007). Yet, the epidemiology of crop diseases and

the inﬂuence of landscape complexity on disease

spread are still largely unknown. Furthermore,

though increased heterogeneity in the landscape

generally increases natural enemy diversity, the

effects on crop pest suppression are highly vari-

able (Karp et al. 2018).

Organisms within agricultural landscapes and

crop susceptibility to herbivores and disease are

also inevitably affected by climate features of the

environment. For crops, temperature variability

and exposure to extreme heat and drought inﬂu-

ence plant physiology, growth, development, and

yield (Prasad et al. 2008, Asseng et al. 2011). Tem-

perature also facilitates the spread and severity of

crop diseases and pathogens through effects on

disease occurrence and development (Colhoun

1973). Extreme temperature ﬂuctuations can

weaken plant defenses to herbivores and disease

(Mattson and Haack 1987, Luck et al. 2011, Raffa

et al. 2013), impact fruit quality, and increase the

likelihood of crop failure (Teixeira et al. 2013).

Increased temperature variability under climate

change is consequently forecasted to reduce crop

yield (Fuhrer 2003, Tubiello et al. 2007, Deutsch

et al. 2018). Some diseases are associated with ele-

vated temperatures, and other diseases are associ-

ated with low temperatures, meaning that

temperature variability impacts pathogen sur-

vival and ﬁtness. Thus, assessing local tempera-

ture variability is necessary to understand how

abiotic factors affect crop plant damage and ulti-

mately sustainable food production.

Conservation biological control is a habitat

management strategy in agroecological farm

design that implements ecological knowledge of

local and landscape biotic and abiotic factors to

promote pest (insect, disease) suppression. Farm

managers utilize knowledge of ecological princi-

ples such as biological diversiﬁcation, structural

complexity, and species interactions to reduce

crop exposure and vulnerability to pests through

intrinsic crop protection by natural enemies and

associated resistance (Heimpel and Mills 2017).

At the local farm scale, conservation biological

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AGROECOSYSTEMS EGERER ET AL.

control practices include incorporating non‐crop

perennials, ﬂoral resources, and agroforestry

(Rusch et al. 2013, Crowder and Jabbour 2014).

At the landscape scale, natural vegetation and

non‐crop land surrounding farms are linked to

insect pest (Tscharntke et al. 2005, 2007, Gardiner

et al. 2009, Martin et al. 2019) and disease regu-

lation through greater landscape complexity

(Plantegenest et al. 2007). Thus, both local to

landscape‐scale management that incorporates

conservation biological control ideas and prac-

tices can provide ecologically based interventions

to reduce crop plant damage and boost yield.

Urban agroecosystems, including urban farms

and gardens, vary greatly in vegetation manage-

ment and urban landscape context, and are often

managed at a much smaller spatial scale than

rural farms, meaning that management strategies

should be very different (Tiffany 2017). Com-

pared to rural agroecosystems, little is known

about crop pests in urban agriculture (Surls et al.

2014). This is problematic because over 60% of

urban farmers report pest‐related challenges

(Oberholtzer et al. 2014) and sustainable pest

management is highly knowledge‐and time‐in-

tensive (Gregory et al. 2015). Consequently,

research‐informed pest management training

and educational materials for urban agriculture

are needed (Surls et al. 2014). Unique biotic and

abiotic characteristics of cities alter bottom‐up

and top‐down forces with potential conse-

quences for herbivore and disease regulation. For

example, irrigation and plant fertilization can

increase host plant quality, beneﬁtting herbivore

populations (Faeth et al. 2005), while warmer

temperatures due to urban heat islands increase

herbivore fecundity and pathogen spread, lower-

ing effectiveness of natural enemies (Raupp et al.

2010, Dale and Frank 2014). Natural enemies,

which depend on natural areas for alternative

resources and overwintering sites (Landis et al.

2000), are often negatively affected by urbaniza-

tion (Fenoglio et al. 2013), and urban tempera-

ture extremes can reduce top‐down regulation

(Meineke et al. 2014). However, the combined

effects of changes in microclimate, local vegeta-

tion management, and landscape context on crop

pests, natural enemies, and crop plant damage in

urban agroecosystems remain unclear. This infor-

mation is crucial given the limited set of pest con-

trol options (e.g., non‐chemical) and fewer

grower support and resources (e.g., the Coopera-

tive Extension Service) designed for urban agri-

culture (Reynolds 2011, Surls et al. 2014).

In this study, we aimed to improve our ecolog-

ical understanding of the local and landscape fac-

tors affecting crop plant damage in urban

agroecosystems across an urban landscape in

California, USA. We speciﬁcally examined the

effects of local vegetation management, local

temperature variability, and surrounding land-

scape context on crop plant damage by insect

herbivores and disease. To do so, we used three

common crops in urban agroecosystems as a

model system to ask how these local and land-

scape factors relate to different types of common

plant damage by herbivores and disease over the

growing season. We asked: (1) How do local

agroecosystem vegetation management factors,

local temperature variability, and landscape con-

text (the amount of natural habitat in the sur-

rounding landscape) affect plant damage on cole

crops (Brassica oleraceae), cucurbits, and toma-

toes? Is there an interaction between local and

landscape factors? (2) Do these factors differen-

tially affect herbivore versus disease plant dam-

age? We tested the hypotheses: (1) Plant damage

will be lower in more vegetatively heterogenous

urban agroecosystems than in homogenous ones;

(2) plant damage will be lower when the agroe-

cosystems are embedded in more complex urban

landscapes with greater amounts of natural habi-

tat land cover; (3) there will be an interaction

between local and landscape effects (i.e., the

effect of local factors will depend on landscape

context), where the positive effects of local fac-

tors will be higher in less complex landscapes

with less natural cover; (4) plant damage will be

lower in urban agroecosystems with less variable

temperatures due to less exposure to tempera-

ture extremes; and (5) the effects of local vegeta-

tion, temperature, and landscape factors vary

with herbivore versus disease damage.

METHODS

Study system

We worked in 24 urban community gardens

(henceforth “gardens”) in three counties in the

California central coast, USA: Monterey

(36.2400″N, 121.3100″W), Santa Clara (37.3600″

N, 121.9700″W), and Santa Cruz (37.0300″N,

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AGROECOSYSTEMS EGERER ET AL.

122.0100″W; Appendix S1: Fig. S1). The gardens

ranged from 405 to 15,525 m

in size, were sepa-

rated from one another by >2 km, and were sur-

rounded by a mix of natural (e.g., forest, grass,

shrub), agricultural (e.g., crop, pasture), open

green space (e.g., parks, golf courses), and urban

impervious land cover (Egerer et al. 2017a). We

chose gardens that varied both in surrounding

landscape factors and in local management fac-

tors (e.g., vegetation composition and structure,

ground cover). All gardens are managed toward

the cultivation of organic produce; however,

agricultural practices and pest management

strategies (e.g., hand removal and biologically

based products) differ between gardens and may

inﬂuence our results. Within each garden, we

concentrated sample efforts within a 20 920 m

plot at the center of each garden. We sampled

gardens at three sampling periods across the

growing season (June 25–28, July 16–19, August

6–9, 2018).

Plant damage

We studied plant damage from herbivores and

diseases on three common crop plant species in

our study system: cole crops (Brassica oleracea;

henceforth “Brassica”), cucurbits (squash, cucum-

ber, melons; Cucurbita pepo), and tomato (Sola-

num lycopersicum). We chose three different crop

species as a model system because they are com-

mon crops found in all gardens and experience

different forms of plant damage. We measured

plant damage using crop‐speciﬁc techniques

(Table 1). At each of the three sampling periods,

we randomly selected individuals of each of the

focal crop species in each garden (n=20 cole

crop individuals; n=3 cucurbits; n=3 toma-

toes). The sampled plants were not the same

across all three sampling periods, and sample

size varied with plant availability at a site. In

addition, the presence of crop varieties varied

across the site, meaning that we could not control

sampling for varietal differences. Therefore, all

analyses consider crop species, regardless of vari-

ety. For Brassica, we randomly selected two

leaves per plant (top, bottom) and using a trans-

parency ﬁlm with a 2 92 cm grid counted (1)

squares with damage from chewing, sucking,

and mining herbivore insects and (2) squares

with disease damage (identifying the disease if

possible). We also measured the plant height and

width. For cucurbits, we counted (1) leaves with

and without powdery mildew and (2) fruits with

and without mildew, sun, or herbivore (mam-

mal) damage. For tomatoes, we counted fruits

with and without disease, sun, or herbivore

(bird) damage. We also collected data on the total

number of healthy and damaged tomato and

cucurbit plants in the 20 920 m plot (e.g., gar-

den scale in Table 1) to assess disease damage

from tomato wilt and powdery mildew. We

counted the number of all Brassica, cucurbit, and

tomato plants within the 20 920 m plot as a

measure of conspeciﬁc density.

On each sampled cucurbit plant, we recorded

the presence of Psyllobora vigintimaculata—a fun-

gus eating lady beetle natural enemy. We did this

because previous investigations suggested that

this species is associated with mildew on plants

and could be providing disease regulation

(Egerer et al. 2016). Thus, this measurement was

designed to obtain a quick assessment of natural

Table 1. The three focal crop species in this study and their common forms of plant damage, both leaves and

fruits, sampled in this study and the sampling effort for each crop.

Focal crop Leaf damage Fruit damage Sampling effort

Cole crop

(Brassica)

Herbivory (insect):

chewing, sucking, mining

herbivory

NA 20 plants 93 sampling periods = 60/site

Bacterial and fungal

disease: leaf spot, rot,

mildew, rust

Cucurbit Powdery mildew Chewing

herbivory (insect)

Herbivory (mammal)

Sun scorch

Mildew

(a) 3 plants 93 sampling periods = 9/site

(b) Diseased vs healthy in site (20 m

)93 sampling

periods

Tomato Tomato wilt (Fusarium and

Verticillium wilt)

Herbivory (bird) Disease

Sun scorch

Mildew

(a) 3 plants 93 sampling periods = 9/site

(b) Diseased vs healthy in site (20 m

)93 sampling

periods

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AGROECOSYSTEMS EGERER ET AL.

enemy presence in relation to mildew abundance

to inform potential pest regulation by natural

enemies on a crop plant.

Local vegetation management, temperature, and

landscape factors

Within each garden, we collected information

on local vegetation and ground cover, tempera-

ture, and the amount of natural habitat cover in

the surrounding landscape as hypothesized fac-

tors that affect plant damage (Table 2; Fig. 1).

For local vegetation management factors, we

measured local vegetation and ground cover fac-

tors at each sampling period. In each garden,

within the 20 920 m sampling plot, we ran-

domly placed eight 1 91 m quadrats within

which we identiﬁed all herbaceous plants (except

grasses) to morphospecies, counted all ﬂowers,

and assessed percent ground cover of

mulch woodchips (a common ground cover

amendment used to suppress weedy vegetation).

We counted and identiﬁed all trees and shrubs in

the garden. In addition, we estimated the total

garden size (m

) using Google Earth imagery

because agroecosystem size can considerably

affect communities of insects and plants.

For the local temperature factor, we measured

the variability in temperature within each garden

with a temperature logger (Onset HOBO UA‐

001‐08; 5.8 93.3 92.3 cm in size, 8 K in Mem-

ory; www.onsetcomp.com/products/data-logge

rs/ua-001-08). The loggers have an operating

range of −2°–70°C, an accuracy of ±0.53°C within

0°–50°C, and a temperature resolution of 0.14°C

at 25°C. Three weeks prior to the ﬁrst sampling

period, temperature loggers were placed 1.3 m

above the ground in the center of the garden and

set to record hourly averaged ambient

temperature measurements. Temperature loggers

were protected from ultraviolet radiation with

Table 2. Descriptive statistics for the (a) local and landscape factors measured across the gardens across the sam-

pling period hypothesized to predict plant damage and (b) the plant damage measurements observed across

sampled plants, at each respective scale, in the gardens across the sampling period (b).

Variable Mean SD Min Max

(a) Local and landscape predictor variables

Garden size (acres) 1.1 0.9 0.1 3.8

Temperature variability (temp. SD) 6.3 1.4 3.2 8.9

Arboreal abundance (No. trees and shrubs) 21.5 18.3 0.0 73.0

Vegetation complexity (No. herbaceous plant species) 22.0 6.0 7.0 39.0

Floral abundance (No. ﬂowers within 1 m

) 88.5 152.1 3.8 833.5

Ground cover (% woodchip mulch ground cover within 1 m

) 20.6 18.1 0.0 90.4

Landscape complexity (No. natural land cover; 2 km) 13.9 19.7 0.0 61.2

Conspeciﬁc density (No. Brassica) 41.5 49.2 1.0 220.0

(b) Plant damage response variables

Brassica

Chewing damage (% leaf area) 11.1 15.4 0.0 35.0

Sucking damage (% leaf area) 11.4 17.3 0.0 55.0

Mining damage (% leaf area) 0.6 3.3 0.0 7.0

Disease damage (% leaf area) 4.3 12.0 0.0 50.0

Total damage (% leaf area) 26.9 24.4 0.0 101.0

Cucurbit

Mildew prevalence within garden (% of plants) 34.0 28.0 0.0 100.0

Fruit herbivory (% No. fruits) 1.0 5.0 0.0 33.0

Fruit sun damage (% No. fruits) 4.0 16.0 0.0 100.0

Fruit mildew damage (% No. fruits) 1.0 4.0 0.0 22.0

Leaves with mildew (No. leaves) 11.3 8.8 0.0 37.7

Tomato

Wilt prevalence within garden (% of plants) 22.4 23.1 0.0 87.0

Fruit herbivory (% No. fruits) 2.0 3.0 0.0 10.0

Fruit sun damage (% No. fruits) 0.0 1.0 0.0 7.0

Fruit disease damage (% No. fruits) 1.0 4.0 0.0 26.0

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AGROECOSYSTEMS EGERER ET AL.

white plastic shields fastened over them and

checked throughout the survey period to ensure

no radiation error (Terando et al. 2017). We

downloaded and collected the data at the end of

the study using an Optic USB interface, and qual-

ity checked and cleaned the data. We calculated

interday variation in daily mean temperature for

each garden for each sampling period (i.e., over

the three weeks prior to ﬁeld sampling) based on

standard deviation (SD). This measure of ﬁne

spatial and temporal scale temperature variabil-

ity was used as explanatory factor for predicting

differences in plant damage.

For the landscape factor, we used land cover

data from the US Geological Survey’s National

Land Cover Database (NLCD; Jin et al. 2013) at

30‐m spatial resolution to measure the propor-

tion of natural and semi‐natural land cover

(henceforth natural land cover for simplicity)

within buffers at a 2‐km spatial scale surround-

ing each garden. We deﬁne natural land cover to

be the total of deciduous (NLCD number 41),

evergreen (42), and mixed forests (43), dwarf

scrub (51), shrub/scrub (52), and grassland/

herbaceous (71) vegetation. We focused on the

amount of natural land cover within 2 km as a

landscape‐scale factor because it is an indicator

of landscape complexity and local on‐farm biodi-

versity in most pest control and agroecology

studies (Tscharntke et al. 2007, Martin et al.

2016, Karp et al. 2018). Using spatial statistics

tools in ArcGIS (v 10.1; ESRI 2011), zonal his-

tograms identiﬁed the total proportion cover of

the NLCD natural land cover classes present

within each buffer. Here, a high total proportion

of natural land cover in the landscape indicates

high landscape complexity, and a low proportion

indicates low landscape complexity.

Analysis

To test how differences in local vegetation,

temperature, and landscape factors predict plant

damage (Table 2), we built mixed effects models

for each focal crop (Brassica, cucurbit, tomato)

informed by our hypothesized relationships

(Fig. 1). We analyzed ten types of plant damage

across the three crops: four variables for Brassica

at the plant scale, two variables for cucurbits at

the plant and garden scale, and three variables

for tomatoes at the plant and garden scale.

Fig. 1. Measured local vegetation and temperature factors in the gardens (a) and a landscape factor (b) that repre-

sent the predicted effects of local and landscape factors on observed plant damage of leaves and fruits for three com-

mon crops (c) in urban agroecosystems (community gardens). Dashed line connecting herbaceous plant species

diversity and the amount of natural habitat land cover within 2 km in the landscape represents the interaction

between local and landscape factors tested in the model. Images courtesy of the University of California Integrated

nia; licensed under the Creative Commons Attribution-NonCommercial-No Derivatives 4.0 International License).

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AGROECOSYSTEMS EGERER ET AL.

Mining damage on Brassica, fruit damage on

cucurbits, and sun and disease tomato fruit dam-

age were negligible (Table 2), so we did not ana-

lyze these data. The dependent variables for each

crop plant included all of the local and landscape

factors as covariates and an interaction term

between the number of herbaceous plant species

and natural land cover in the landscape to test

for a signiﬁcant local–landscape interaction. We

included sampling date and garden site as ran-

dom effects in all models.

For Brassica, we created four response vari-

ables to analyze (1) amount of leaf damage from

insect chewing damage (mean leaf area with

chewing damage), (2) amount of leaf damage

from insect sucking damage, (3) amount of leaf

damage from disease damage, and (4) amount of

total leaf damage. To test how local and land-

scape factors predict Brassica damage, we the

modeled the average amount of leaf area dam-

aged from chewing, sucking (log‐transformed),

and disease (log‐transformed) per site per sam-

pling period as the response variable using a

Gaussian distribution in generalized linear

mixed models (GLMMs) and linear mixed mod-

els (LMM). The models included Brassica con-

speciﬁc density within the garden as a covariate

and average plant volume (height 9width) as

offset term to account for sampling area. An off-

set term is a known component of the linear pre-

dictor variable that requires no coefﬁcient

(McCullagh and Nelder 1989).

For cucurbits, we created two response vari-

ables to test how local and landscape factors pre-

dict cucurbit damage at the plant scale and

garden scale: (1) log‐transformed pooled average

number of leaves with powdery mildew damage

per site per sampling period (plant scale) and (2)

the number of plants with powdery mildew and

plants without powdery mildew within the gar-

den (garden scale). For the plant scale model, we

ﬁt the full model with a Gaussian distribution in

a LMM. For the garden scale model, we used the

cbind function to create a matrix of the number

of plants with powdery mildew and without

powdery mildew as the response and ﬁt the

model with a Binomial distribution in a GLMM.

To test whether natural enemy presence predicts

plant damage, we similarly modeled the number

of leaves with powdery mildew with the pres-

ence of Psyllobora as the covariate in a LMM.

For tomatoes, we created three response vari-

ables to test how local and landscape factors pre-

dict tomato damage at the plant scale and

garden scale: (1) pooled average of fruits with

herbivory damage (plant scale); (2) pooled aver-

age values of all fruit damage (herbivory, disease,

sun) across the site (plant scale); and (3) the num-

ber of plants with and without wilt within the

garden (garden scale). For plot scale fruit dam-

age, we log‐transformed plant scale values and

we removed three sites where there were no con-

sistent numbers of tomato individuals to sample

to maintain our random effects. For the garden

scale model, we used the cbind function to create

a matrix of the number of plants with wilt and

plants without wilt as the response and ﬁt the

model with a Binomial distribution in a GLMM.

For each full model for each crop plant, we

performed model selection using the dredge

function in the R package MuMIn (Barton 2009).

The method ﬁts all possible combinations of

models of the covariates and compares their abil-

ity to best explain or predict the response vari-

able—in this case the amount of leaf or fruit

damage for each crop type—using the Akaike

information criterion (AICc). The explanatory

variables (local vegetation, temperature, land-

scape factors) were scaled in the models, and VIF

scores for all models were <3. Signiﬁcance of the

explanatory variables is taken at p≤0.05. Model

ﬁt for each model was estimated using AIC

rela-

tive to a null model (Burnham and Anderson

2002). Analyses were performed in the R statisti-

cal environment (R Development Core Team

2016).

RESULTS

Plant damage on Brassica, cucurbits, and toma-

toes varies in form and in magnitude across the

gardens (Tables 2, 3). The percent of leaf area

damaged on Brassica highly varied across all

sampled plants and by damage type (Table 2).

The most prevalent disease damage on Brassica

included white spot, bacterial leaf spot, and

white rust (Table 3). Powdery mildew damage

on cucurbit leaves was prevalent, but fruit dam-

age was minimal. Of 180 sampled cucurbit plants

across the season, 58.9% had powdery mildew

damage on their leaves. Few plants had sun, her-

bivore, or mildew damage; in only one case, a

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AGROECOSYSTEMS EGERER ET AL.

plant had both fruit herbivory and sun damage.

Fruit damage on sampled tomato plants

included herbivory, disease, and sun scorch. The

most prevalent diseases on tomato included late

blight, black mold, and bacterial leaf spot

(Table 3). The proportion of tomatoes with dis-

ease ranged from 0% to 87% of plants, with an

average of about a quarter of plants. Disease

damage was seasonal and only observed in the

late summer season (August). The prevalence of

powdery mildew on cucurbits and tomato dis-

ease (wilt) in the gardens highly varied across

sites. The proportion of cucurbits with powdery

mildew at the garden scale ranged from 0% to

100% of plants at a site, but on average about a

third of plants had mildew. While we present

results from total plant damage as this may be

important to production‐focused practitioners,

we focus on the speciﬁc types of plant damage in

our results and discussion.

Local and landscape predictors of plant damage

The differences in local vegetation, tempera-

ture, and landscape factors variably predicted

plant damage measures among the three focal

crops (Table 4; Fig. 2).

For Brassica, the best model predicting the

amount of chewing leaf damage included the

number of herbaceous plant species in the garden,

while the best model predicting the amount of dis-

eased leaf damage included temperature variabil-

ity, the amount of natural cover, and garden size.

Leaf area of disease damage was signiﬁcantly

lower in gardens with more variable temperatures,

in smaller gardens, and in gardens surrounded by

more natural cover within 2 km. No factors pre-

dicted sucking damage and total leaf damage well,

and the best model was the null model.

For cucurbits, the best model predicting the

number of leaves with powdery mildew at the

plant scale included ﬂoral abundance,

Table 3. Disease damage observed on focal plant species (Brassica, cucurbit, tomato) within the 24 gardens across

the sampling period.

Crop

Causal

Agent Scientiﬁc Name Common Name N%

Brassica Bacteria Pseudomonas syringae Bacterial leaf spot 51 18.41

Bacteria Xanthomonas campestris Black rot 27 9.75

Bacteria/

Fungi

Alternaria; Alternaria brassicae Leaf spot 10 3.61

Fungi Pseudocercosporella capsellae White spot 81 29.24

Fungi Fusarium oxysporum Fusarium yellows 24 8.66

Fungi Peronospora parasitica Downy mildew 22 7.94

Fungi Erysiphe cruciferarum Powdery mildew 7 2.53

Fungi Mycosphaerella brassicicola Ring spot 7 2.53

Fungi Phytophthora megasperma Root rot; Phytophthora root

rot

2 0.72

Fungi Sclerotinia White rot 1 0.36

Fungi Capnodium spp., Fumago spp., others Sooty mold 1 0.36

Oomycete Albugo candida White rust 43 15.52

Cucurbit Fungi Podosphaera xanthii; Erysiphe cichoracearum Powdery mildew 106;

934*

58.9

Tomato Bacteria Xanthomonas campestris pv. Vesicatoria Bacterial leaf spot 2 16.67

Fungi Phytophthora infestans Late blight 4 33.33

Fungi Alternaria alternata Black mold 3 25.00

Viral Phytophthora Black rot 1 8.33

Fungi Alternaria solani Early blight 1 8.33

Fungi Tospovirus Spotted wilt virus 1 8.33

Fungi Fusarium oxysporum f. sp. lycopersici; Verticillium

dahliae

Fusarium wilt; Verticillium

wilt

1047†12.78

Notes: Data are the total number of individuals observed on all sampled plants (N) and the percentage of that cause of dis-

ease damage on the plants by focal crop (%). Note that tomato and cucurbit include garden scale measurements.

* Count of total number of cucurbit plants at the garden scale across all sampling periods.

†Count of total number of plants with disease at the garden scale across all sampling periods.

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AGROECOSYSTEMS EGERER ET AL.

herbaceous plant species richness, and the

amount of natural cover. Leaf powdery mildew

on plants was signiﬁcantly lower in gardens with

more ﬂowers and surrounded by more natural

cover, but signiﬁcantly higher in gardens with

more herbaceous plant species. In addition, the

presence of Psyllobora lady beetles on cucurbit

plants was signiﬁcantly positively correlated

with the average number of leaves with powdery

mildew. At the garden scale, the proportion of

cucurbit plants with powdery mildew was best

predicted by temperature variability, ﬂoral

abundance, herbaceous plant species, the num-

ber of trees and shrubs, garden size, and the

amount of natural land cover in the landscape.

The proportion of cucurbit plants with mildew

was signiﬁcantly higher in gardens with more

variable temperatures and more herbaceous

plant species, whereas it was signiﬁcantly lower

in gardens with more ﬂowers, in larger gardens,

and in gardens surrounded by more natural land

cover.

For tomatoes, the best model predicting

tomato herbivory fruit damage included the

Table 4. Results of the mixed models built with local and landscape factors that best predicted plant damage

measures for the three focal crop plant species determined using model selection.

Crop and scale Response Predictor Coefﬁcient SE

Adj

zPAIC

Brassica Plant Chewing damage Intercept 2.92 0.27 10.74 <0.001 223.36

Herb. Plant Spp −0.40 0.22 1.77 0.08

Sucking damage (log)†Intercept 1.22 0.25 4.80 <0.001 132.80

No. Trees and shrubs 0.12 0.10 1.20 0.23

Disease damage (log) Intercept 0.04 0.22 0.16 0.87 190.22

Temp SD 0.52 0.23 2.26 0.02

% Natural cover (2 km) −0.60 0.26 2.28 0.02

Garden size −0.46 0.22 2.04 0.04

Total leaf damage (log)†Intercept 2.00 0.11 17.80 <0.001 109.74

% Woodchip mulch −0.09 0.07 1.23 0.22

Cucurbit Plant Leaf powdery mildew (log) Intercept 2.13 0.32 6.71 <0.001 160.43

No. Flowers −0.25 0.10 2.36 0.02

Herb Plant Spp 0.42 0.11 3.76 <0.001

% Natural cover (2 km) −0.39 0.12 3.43 <0.001

Leaf powdery mildew (log) Intercept 2.03 49.00 12.02 <0.001 160.43

No. Psyllobora 0.42 49.00 2.36 0.02

Garden Damaged : Healthy plants Intercept −0.87 0.66 1.31 0.19 369.80

Temp SD 0.33 0.13 2.60 0.01

No. Flowers −0.35 0.08 4.54 <0.001

Herb Plant Spp 0.21 0.08 2.65 0.01

% Natural cover (2 km) −0.63 0.13 4.69 <0.001

Garden size −0.48 0.14 3.48 <0.001

No. Trees and shrubs 0.07 0.12 0.62 0.53

Tomato Plant Fruit herbivory damage (log) Intercept −1.73 0.01 140.58 <0.001 63.67

No. Trees and shrubs −0.72 0.01 69.17 <0.001

Temp SD 0.15 0.01 23.84 <0.001

Fruit damage Intercept −1.09 0.54 2.01 0.04 85.63

No. Trees and shrubs −0.40 0.23 1.73 0.08

Garden Damaged : Healthy plants Intercept −1.73 0.54 3.24 0.001 412.03

Herb Plant Spp 0.23 0.08 2.67 0.008

% Natural cover (2 km) 0.11 0.23 0.49 0.63

Local 9Landscape 0.34 0.08 4.50 <0.001

% Woodchip mulch −0.12 0.14 0.84 0.40

Notes: See text and Table 2 for details on variables used in the analysis. Local 9Landscape indicates interaction term

between the number of herbaceous plant species and the amount of natural habitat land cover in the landscape within 2 km

surrounding a garden. Colon (:) indicates the proportion of damaged to healthy plants. Coeff., coefﬁcient; SE

Adj

, standard error

(adjusted); SD, standard deviation; z,z‐value; P, P‐value at 95% conﬁdence; and AIC

, Akaike’s information criterion for small

sample size.

†Best ﬁt model with lowest AIC

was the null model; we present next best ﬁt model.

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AGROECOSYSTEMS EGERER ET AL.

number of trees and shrubs and temperature

variability. Tomato herbivory fruit damage was

signiﬁcantly higher in gardens with fewer trees

and shrubs, and with more variable tempera-

tures. The best model predicting all fruit damage

included the number of trees and shrubs. At the

garden scale, the proportion of tomatoes with

tomato wilt disease was best predicted by the

number of herbaceous plant species, mulch

woodchip ground cover, the amount of natural

land cover in the landscape, and the interaction

between herbaceous plant species and natural

land cover. The proportion of tomato plants with

wilt disease was signiﬁcantly higher in gardens

with more herbaceous plant species and sur-

rounded by more natural land cover, with the

positive effect of herbaceous plant species

increasing with increasing with greater amounts

of natural land cover in the landscape.

DISCUSSION

We investigated local and landscape factors

associated with plant damage on three common

crop species in urban agroecosystems using

urban community gardens as a model system.

We found that local and landscape factors signiﬁ-

cantly predict herbivore and disease damage, but

that the importance of these factors and the

direction of the association vary with crop spe-

cies and damage type. We discuss the biotic and

abiotic local and landscape factors associated

with plant damage and the urban agroecological

applications.

Local and landscape factors predict plant damage

In support of our hypotheses, higher amounts

of local vegetation complexity (e.g., trees and

shrubs) and landscape complexity (percent natu-

ral land cover) are associated with lower inci-

dence of some measures of herbivore and disease

damage in gardens. Speciﬁcally, we found that

tomato fruit damage from herbivores and disease

was lower in gardens with more trees and

shrubs, powdery mildew prevalence is lower in

gardens with more ﬂowers, and amounts of

chewing damage on Brassica leaves are lower in

gardens with more herbaceous plant species.

Arboreal vegetation through agroforestry may

enhance agroecosystem structural complexity,

Fig. 2. Simpliﬁed visual summary of the relationships between plant damage measures and local vegetation,

temperature, and landscape factors (top x‐axis) at either the plant or garden scale for each of the focal crop spe-

cies (y‐axis) of Brassica (a), cucurbits (b), and tomato (c). Important factors from the best models are represented

by gray circles, where size of the gray circle represents the degree of signiﬁcance (larger circles P<0.01; smaller

circles 0.01 <P<0.05). Directionality of signiﬁcant factors shown within circles as either positive (+) or negative

(−), with insigniﬁcant factors in models represented as directionality within parentheses ((+)) and no circle. Text

below circles indicates disease type (“chewing,”“mildew,”etc.). Models shown are at the plant scale (a), at the

garden scale (b), or at both scales (c). See Table 4 for model results for further interpretation.

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AGROECOSYSTEMS EGERER ET AL.

provide alternative food resources to divert

potential crop herbivores, and moderate micro-

climate to reduce disease prevalence both above

and below ground (Pumarino et al. 2015). More

plant diversity through ﬂowering plants may

provide food resources for natural enemies that

protect plants from insect and pathogen pests.

Although we did not measure top‐down pest

regulation, these ﬁndings seem to support agroe-

cological theories and conservation biological

control practices positing that greater habitat

heterogeneity through structural and functional

diversiﬁcation can promote pest control by low-

ering resource concentration for herbivores and

boosting natural enemies (Altieri et al. 1983,

Altieri 2002).

Yet, we found mixed effects of herbaceous

plant species richness in regard to crop disease

damage, supporting the argument that increas-

ing plant diversity to mitigate pest impacts is not

a straightforward management guideline in

urban environments (Dale and Frank 2018). Both

powdery mildew and tomato wilt at the garden

scale were more prevalent in gardens with more

herbaceous plant species. The epidemiology of

crop disease predicts that crop mixtures should

dampen disease epidemics by reducing disease

spread likelihood between conspeciﬁc plants.

However, the presence of one highly susceptible

reservoir species could increase pathogen preva-

lence of other species through pathogen spillover

(Power and Mitchell 2004). Thus, disease out-

breaks may increase within agroecosystems if

plant species are introduced that harbor or are

vulnerable to certain diseases shared by other

crop species within the system. The spatial distri-

butions and phylogenetic relatedness of different

plant species may also be important for manag-

ing disease outbreaks (Schroth et al. 2000). In our

case, even a few garden plots with only cucurbits

or only tomatoes could act as pathogen sources

to surrounding plots, even if those plots are

themselves specious. Habitat size could mitigate

these effects through dilution and pathogen dis-

persal limitation, and this could explain why gar-

den size reduces powdery mildew prevalence at

the garden scale. Within a crop type, varietal dif-

ferences in terms of resistance to insects and

pathogens may also be important for inﬂuencing

plant resistance to insects and pathogens (Wolfe

1985, Zhu et al. 2000). Community gardens are

thus complex from an epidemiological perspec-

tive because they harbor many plant species

(e.g., food crops, exotic ornamentals, and native

vegetation) and varieties (e.g., heirloom toma-

toes, cultivars of burpless cucumbers, kale vari-

eties) and interspeciﬁc plant interactions.

Furthermore, pest spread within the garden

depends on the management decisions and prac-

tices used by many people. Future studies should

investigate how varietal differences, spatial dis-

tribution, and different management strategies

inﬂuence plant damage within urban production

systems.

We found that plant damage in urban agroe-

cosystems is also associated with landscape con-

text and that effects of local factors can depend

on landscape context. In accordance with our

hypothesis, gardens surrounded by more natural

land cover had lower cucurbit powdery mildew

prevalence and less Brassica disease leaf damage.

In urban landscapes, plant pathogen outbreaks

can heighten with increased urbanization due to

loss of native forest cover and introduced orna-

mental plant species harboring pathogens (Paap

et al. 2017, Roman et al. 2018), or novel insect

pests associated with fungal pathogens that bur-

geon in urban areas (Ploetz et al. 2013, O’Don-

nell et al. 2016). The results here on disease

damage suggest that natural habitat within the

landscape is (1) reducing pathogen dispersal and

there are fewer source habitats for crop diseases

in these landscapes or (2) supporting natural ene-

mies that provide top‐down disease control

(Plantegenest et al. 2007). We found an impor-

tant interaction between local and landscape fac-

tors on tomato wilt prevalence in gardens, where

the positive effect of herbaceous plant species on

wilt prevalence increased in gardens surrounded

by more natural land cover. The positive interac-

tion on tomato disease prevalence is interesting

because tomato fungal and viral diseases (e.g.,

fusarium wilt and verticillium wilt) are often

soil‐borne and moisture‐dependent (see below).

Many of the gardens in more complex land-

scapes surrounded by more natural land cover

receive more coastal fog or are located in agricul-

tural regions, suggesting that other abiotic or cul-

tural factors including fog‐facilitated dispersal

and land use history are important. Though the

inﬂuence of landscape context on crop disease

spread in urban landscapes is largely unknown,

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AGROECOSYSTEMS EGERER ET AL.

urban agroecosystems may face more challenges

managing certain bacterial and fungal diseases

with increasing urbanization (densiﬁcation and

expansion) and the loss of (semi‐)natural habi-

tats.

We found some differences in how local and

landscape factors are associated with plant dam-

age from herbivores of different feeding guilds.

Chewing damage on Brassica decreased with

increasing herbaceous plant species, while suck-

ing damage generally was higher with higher

abundance of trees and shrubs. In urban green-

spaces, the response of herbivores to vegetation

management can be species‐speciﬁc or feeding‐

guild‐speciﬁc (Raupp et al. 2010). For example,

on golf courses, residential gardens, and parks,

herbivores positively associate with vegetation

volume, but the association with vegetation

diversity within the habitat depends on the par-

ticular herbivore species and presumably their

functional traits along with plant species identity

(Mata et al. 2017). It is surprising that we found

no association between the landscape and Bras-

sica herbivore damage, because our previous

work has linked lower pest regulation of herbi-

vores in gardens surrounded by more urban and

agricultural land cover (and less natural land

cover) in the landscape (Philpott and Bichier

2017). Furthermore, scale insects, aphids, mites,

and leaf miners often increase in urban areas due

to dispersal limitation and higher fecundity, and

the loss of their natural enemies that provide

top‐down control (Shrewsbury and Raupp 2006,

Raupp et al. 2010). Other studies have also

shown increased mining damage (Kozlov et al.

2017) and increased chewing damage (Cuevas‐

Reyes et al. 2013) in more urban areas, though

opposite trends have also been found (Moreira

et al. 2019). In sum, our results further exemplify

the complex, often non‐linear relationships

between ecological factors, herbivores, and her-

bivory in urban environments (Raupp et al.

2010, Dale and Frank 2018).

Temperature variability and plant damage

In our study, greater temperature variability

within urban agroecosystems associated with

higher plant damage, particularly by plant dis-

eases, demonstrating that changes in local micro-

climate are also important for disease dynamics.

More variable temperatures were overall

associated with higher amounts of plant damage

from disease and mildew across crop species.

Here, urban agroecosystems that experience

higher temperatures or greater interday variation

in temperatures are exposed to more extreme

heat. Powdery mildew and tomato wilt preva-

lence at the garden scale and the amount of Bras-

sica disease damage on plants were higher in

gardens with more variable temperatures. The

biology of crop plant diseases could explain

these different responses. For example, fungal

disease spread via spore dispersal is dependent

on temperature and moisture in the environment

(Colhoun 1973). Powdery mildew thrives in war-

mer and drier conditions rather than moist and

cool conditions, whereas several Brassica diseases

disperse through air moisture and depend on soil

temperature and moisture (Koike and Subbarao

2003). Gardens that are in denser, built‐up areas

with more urban cover may be less susceptible to

some crop diseases if those gardens are less likely

to experience pathogen colonization through

wind and moisture. Interestingly, tomato herbi-

vore fruit damage by small mammals and birds

was also higher in gardens with more variable

temperatures. This suggests that more variable

conditions of greater temperature extremes may

either increase foraging activity of herbivores or

alter herbivore foraging strategy if more variable

weather patterns cause risk‐sensitive foraging

behavior (Caraco et al. 1990, Monaco and Hel-

muth 2011). The results here support urban agri-

culture ﬁndings in southern cities where crop

exposure to high temperature extremes can

increase susceptibility to herbivores and disease

(Eriksen‐Hamel and Danso 2010). In the urban

forest, tree species are still susceptible to pests

under extreme heat despite intensive manage-

ment (Kendal et al. 2018). This is because even

short‐term exposure to extremes can have large

and long‐term impacts on crops through effects

on herbivore and disease pest ecology (Coakley

1988, Rosenzweig et al. 2001, Bale et al. 2002).

Thus, even if urban farmers and gardeners read-

ily respond to changing weather patterns to

maintain their plants, temperature still plays an

important role in disease dynamics, crop sur-

vival, and food production. Temperature impacts

on crops have implications for urban agriculture

in relation to climate change, particularly in cities

in California where temperatures and weather

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AGROECOSYSTEMS EGERER ET AL.

events (heat, drought) are becoming more

extreme.

Natural enemies and plant damage

We documented a strong positive association

of Psyllobora—a mycophagous (fungus‐feeding)

lady beetle—with the presence of powdery

mildew on cucurbits. Natural enemies and antag-

onists in agroecosystems are population regula-

tion mechanisms that provide system‐level

resilience to pests and disease (Bianchi et al. 2006,

Vandermeer et al. 2010). The positive association

between Psyllobora and powdery mildew shows a

density‐dependent response of natural enemies

to pest outbreaks, similarly demonstrated in

greenhouse studies (Sutherland and Parrella

2009). Powdery mildews are an important plant

pathogen in agriculture that cause signiﬁcant

yield losses in cucurbits (Miller et al. 2003), and

many gardeners in our system use homemade

bicarbonate solution with baking soda to prevent

mildew establishment on cucurbits. We cannot

determine from our study if higher Psyllobora

densities translate to effective control of powdery

mildew because we did not measure disease

removal. Nor can we provide support for the ene-

mies hypothesis because, while greater plant

cover and species richness can promote natural

enemies, powdery mildew positively associated

with herbaceous plant species richness. Thus, the

mechanisms underlying powdery mildew control

in this system are unclear.

Although we did not speciﬁcally test this, the

effects of local and landscape factors on herbi-

vore damage could be a result of top‐down indi-

rect effects. Many of the diverse array of natural

enemies in these agroecosystems, including those

from Araneae, Aves, Carabidae, Coccinellidae,

and Hymenoptera, are affected by local factors,

such as vegetation diversity and composition,

and by landscape factors, such as landscape com-

position (Otoshi et al. 2015, Burks and Philpott

2017, Egerer et al. 2017b, 2018, Philpott et al.

2019). In addition, experimental work in these

systems indicates that pest removal is also

affected by garden ground cover, vegetation

(complexity, diversity), and landscape context

(Philpott and Bichier 2017). Thus, in this study,

the low leaf damage of Brassica plants in gardens

with more woodchip mulch and more herba-

ceous plant species could be explained by the

effects that these factors have on natural enemies

that then cascade down to herbivores and, ulti-

mately, to plant damage. In fact, the amount of

woodchip mulch and herbaceous plant species

positively correlates with higher activity of

ground‐dwelling spiders and carabid beetles in

these agroecosystems (Otoshi et al. 2015, Philpott

et al. 2019). It is interesting that we found lower

fruit damage in gardens with more arboreal veg-

etation because agroforests may support mam-

mal and bird pests (Pumarino et al. 2015). Soil

management practices and water use by garden-

ers may also affect pest outbreaks and pest regu-

lation in gardens through effects on plant

condition (e.g., plant size, nutrient content, water

stress; Archer et al. 1995), to increase likelihood

of plant damage (Kim and Underwood 2015). In

our system, soil‐related factors only indirectly

affect herbivore pest regulation through direct

effects on plant volume (Egerer et al. 2018).

Because we accounted for plant size in our analy-

sis, we cannot make strong linkages between soil

and water management and crop damage here.

In sum, though agroecosystems are in constant

ecological ﬂux and our sampling for one natural

enemy species (and plant damage in one season)

captures a static measure of a dynamic process in

relation to certain local and landscape factors,

this work informs the ecology of plant damage

and protection in urban contexts.

Agroecological applications

Urban farmers and gardeners face unique chal-

lenges in their efforts to produce food crops uti-

lizing agroecological methods in urban

environments (Altieri et al. 1999, Eriksen‐Hamel

and Danso 2010, Tiffany 2017). Many also report

lack of urban agroecological resources and train-

ing, for example, from Cooperative Extension

Services in the USA (Oberholtzer et al. 2014,

Surls et al. 2014). This study ﬁlls knowledge gaps

because most of these urban farmers (92.4%;

N=189; unpublished data, the authors) report

pest‐related challenges and use hand removal,

homemade sprays and tonics to combat damage

by arthropods, snails, and small mammals (the

authors, unpublished data). Even relatively small

amounts of herbivory such as those documented

in this study (~10%) can determine differences in

plant ﬁtness and reproduction (Crawley 1985).

Perhaps more importantly for the urban farmer

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AGROECOSYSTEMS EGERER ET AL.

and gardener, plant damage may reduce the

amount of marketable or usable food given con-

sumer preferences for damage‐free produce

(Thompson and Kidwell 1998, Yue et al. 2007,

Oberholtzer et al. 2014). Though we did not mea-

sure yield here, we suggest that the ﬁndings

from this work can be applied by people to grow

food in cities using agroecologically based con-

servation biological control practices and to

boost yield production through agroecosystem

vegetation management. Given capacity and

ability, urban farmers and gardeners can incorpo-

rate trees and shrubs (Smith et al. 2006, Gonzá-

lez‐García et al. 2009), provision ﬂoral resources

(Landis et al. 2000, Shrewsbury et al. 2004,

Rebek et al. 2006, Bennett and Gratton 2012),

and create heterogenous ground cover habitat

(Tamburini et al. 2016) for beneﬁcial natural ene-

mies to reduce insect and disease plant damage.

Many of these recommendations in both rural

agricultural and urban ecosystems echo sustain-

able agroecological practices including conserva-

tion biological control for urban agroecosystems

aimed at enhancing local habitats for beneﬁcial

insects and species interactions to promote pest

control (Altieri and Nicholls 2018, Arnold et al.

2019).

Urban farmers must also acknowledge and

manage for the multitude of trade‐offs in their

management decisions. In these heterogenous

systems, effects of abiotic and biotic local and

landscape factors on crop plant damage depend

on crop species and damage type, and different

factors associate with herbivore‐versus disease‐

mediated damage. Practitioners can add wood-

chip ground cover to possibly increase habitat

for spider natural enemies that protect Brassica,

but this habitat feature may detrimentally affect

ground‐nesting pollinators essential to pollina-

tion (Quistberg et al. 2016). Crops may suffer less

insect or disease damage in gardens with more

trees and shrubs (e.g., tomatoes in this study),

but yields could suffer as plant growth and fruit

production are greatly affected by shading

(Cockshull et al. 1992). More stable temperatures

in urban agroecosystems may allow for more

species to grow due to less exposure to extremes

(Egerer et al. 2019), but more plant species rich-

ness may lead to pathogen spillover from suscep-

tible disease hosts. Thus, various designs of local

agroecosystems lead to different ecological

interactions (either positive or negative) at multi-

ple scales, with different effects on crop produc-

tion and ecosystem service synergies (Smukler

et al. 2012). This work highlights some of these

management complexities by studying three

physiologically different crops. Utilizing basic

agroecological practices in combination with

local knowledge of the environment should aim

to optimize damage reduction, increase accept-

able production levels, and overall improve sus-

tainable urban food production.

CONCLUSION

Ecological theories in agroecology predict that

system‐level resilience to insect and disease

pests occurs through mechanisms including

greater habitat structural and functional diver-

sity, and the maintenance of natural enemies.

Agroecosystems that incorporate more struc-

tural complexity and diversity through diverse

plant assemblages, and functional diversity

through greater ﬂoral and arboreal vegetation

should better maintain an ecological equilibrium

necessary for urban food production. Our work

shows that urban agroecosystems are vulnerable

to insect and disease pests, but that some local

agroecological diversiﬁcation strategies are asso-

ciated with lower plant damage. Increasing ﬂo-

ral abundance, incorporating agroforestry, and

increasing ground cover heterogeneity are some

of these practices. Yet, urban agroecosystems

are embedded within the social–environmental

context of their broader environment. A combi-

nation of factors largely outside of practitioners

control including agroecosystem size, natural

habitat cover in the surrounding landscape, and

temperature ﬂuctuations all matters for plant

susceptibility to insect and disease pests. Thus,

urban densiﬁcation and climate change will

increasingly challenge urban agroecosystem sus-

tainability and should be considered by urban

planning and policies for urban agriculture.

Nevertheless, it remains crucial to increase habi-

tat heterogeneity and maintain speciose natural

enemy communities in urban agroecosystems to

support intrinsic plant protection. The ability of

local management to combat plant damage

through agroecological approaches will be

essential to ensure the sustainability and pro-

duction capacity of agriculture in cities.

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AGROECOSYSTEMS EGERER ET AL.

ACKNOWLEDGMENTS

We thank the garden organizations that host our

research: Aptos Community Garden, City of San Jose

Parks and Recreation, City of Santa Cruz Parks and

Recreation, Goodwill Community Garden, Homeless

Garden Project, Live Oak Green Grange Community

Garden, MEarth, Mesa Verde Gardens, Mid‐County

Senior Center, Middlebury Institute of International

Studies, Paciﬁc Grove Community Garden, and UC

Santa Cruz. We thank the research support from Ashia

Ajani, Peter Bichier, Brenda Lin, Shalene Jha, Bella

Mayorga, and Justin Suraci. This work was supported

by the US Department of Agriculture [grant number

2016‐67019‐25185 to S.M.P and H.L.]; the National

Science Foundation Graduate Research Fellowship

Program [grant number 2016‐174835 to M.E.]; and the

Environmental Studies Department at the University

of California, Santa Cruz. Thank you to four anony-

mous reviewers for their helpful feedback that signiﬁ-

cantly improved the manuscript. We acknowledge

support by the German Research Foundation and the

Open Access Publication Fund of TU Berlin. We thank

Charlotte Grenier for plant illustrations in Figure 2.

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